{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:50:05Z","timestamp":1787028605320,"version":"build-2736575974"},"reference-count":47,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2024,9,13]],"date-time":"2024-09-13T00:00:00Z","timestamp":1726185600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry for Culture and Innovation","award":["\u00daNKP-23-3"],"award-info":[{"award-number":["\u00daNKP-23-3"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>The Varroa destructor is the most significant bee parasite and the greatest threat to bee health all around the world. Due to its hidden lifestyle, detection within the brood cell is only possible through invasive techniques. Enhancing detection methods is essential for advancing research on population dynamics, spread, selection efforts, and control methodologies against the mite. In our study, we employed infrared imaging to measure the thermal differences in parasite and intact Apis mellifera worker broods. Experiments were conducted over two years at the MATE Kaposv\u00e1r Campus in Hungary involving five beehives in 2022 and five beehives in 2023. A FLIR E5-XT WIFI handheld infrared camera was used to create a heat map of capped brood frames. Our results indicate that the resolution of these cameras is sufficient to provide detailed IR images of a bee colony, making them suitable to detect temperature differences in intact and Varroa parasitized capped brood cells. Mite parasitism causes a time-dependent and sustained temperature increase in developing bee pupae, observable regardless of mite number. Our work demonstrates two different heating patterns: hotspot heating and heating cells that are responsible for the elevated temperature of the Varroa-infested cells as a social fever response by the worker bees. Based on our results, future research combined with AI-based image evaluation software could offer beekeepers and researchers practical and valuable tools for high-throughput, non-invasive Varroa detection in the field.<\/jats:p>","DOI":"10.3390\/insects15090693","type":"journal-article","created":{"date-parts":[[2024,9,13]],"date-time":"2024-09-13T06:39:16Z","timestamp":1726209556000},"page":"693","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Tracking Varroa Parasitism Using Handheld Infrared Cameras: Is Eusocial Fever the Key?"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2569-2720","authenticated-orcid":false,"given":"Tam\u00e1s","family":"Sipos","sequence":"first","affiliation":[{"name":"Department of Agronomy, Institute of Agronomy, Kaposv\u00e1r Campus, Hungarian University of Agriculture and Life Sciences, S. Guba Str. 40, H-7400 Kaposv\u00e1r, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6154-3330","authenticated-orcid":false,"given":"Szilvia","family":"Orsi-Gibics\u00e1r","sequence":"additional","affiliation":[{"name":"Department of Agronomy, Institute of Agronomy, Kaposv\u00e1r Campus, Hungarian University of Agriculture and Life Sciences, S. Guba Str. 40, H-7400 Kaposv\u00e1r, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2170-7315","authenticated-orcid":false,"given":"Tam\u00e1s","family":"Schieszl","sequence":"additional","affiliation":[{"name":"Department of Physiology and Animal Health, Institute of Physiology and Nutrition, Kaposv\u00e1r Campus, Hungarian University of Agriculture and Life Sciences, Guba S\u00e1ndor Str. 40, H-7400 Kaposv\u00e1r, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3276-3347","authenticated-orcid":false,"given":"Tam\u00e1s","family":"Donk\u00f3","sequence":"additional","affiliation":[{"name":"Medicopus Nonprofit Ltd., Guba S\u00e1ndor Str. 40, H-7400 Kaposv\u00e1r, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zsombor","family":"Zakk","sequence":"additional","affiliation":[{"name":"Department of Agronomy, Institute of Agronomy, Kaposv\u00e1r Campus, Hungarian University of Agriculture and Life Sciences, S. 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Behav."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/S0065-2806(06)33003-2","article-title":"Nest thermoregulation in social insects","volume":"33","author":"Jones","year":"2006","journal-title":"Adv. Insect Physiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"7343","DOI":"10.1073\/pnas.1232346100","article-title":"Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development","volume":"100","author":"Tautz","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_4","first-page":"511","article-title":"Respiration of individual honeybee larvae in relation to age and ambient temperature","volume":"174","author":"Petz","year":"2004","journal-title":"J. Comp. Physiol. B"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Stabentheiner, A., Kovac, H., and Brodschneider, R. (2010). Honeybee colony thermoregulation\u2013regulatory mechanisms and contribution of individuals in dependence on age, location and thermal stress. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0008967"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Seeley, T.D. (2009). The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies, Harvard University Press.","DOI":"10.2307\/j.ctv1kz4h15"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1007\/s001140050648","article-title":"Heat shielding: A novel method of colonial thermoregulation in honey bees","volume":"86","author":"Starks","year":"1999","journal-title":"Naturwissenschaften"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4268","DOI":"10.1073\/pnas.0400773101","article-title":"Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development","volume":"101","author":"Groh","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1007\/s00040-017-0573-8","article-title":"A review of impacts of temperature and relative humidity on various activities of honey bees","volume":"64","author":"Owayss","year":"2017","journal-title":"Insectes Sociaux"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1007\/s00359-021-01464-8","article-title":"Coping with the cold and fighting the heat: Thermal homeostasis of a superorganism, the honeybee colony","volume":"207","author":"Stabentheiner","year":"2021","journal-title":"J. Comp. Physiol. A"},{"key":"ref_11","unstructured":"Moritz, R., and Southwick, E.E. (2012). Bees as Superorganisms: An Evolutionary Reality, Springer Science & Business Media."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1080\/0005772X.1955.11094876","article-title":"The water economy and temperature regulation of the honeybee colony","volume":"36","author":"Lindauer","year":"1955","journal-title":"Bee World"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1242\/jeb.91.1.25","article-title":"The mechanisms and energetics of honeybee swarm temperature regulation","volume":"91","author":"Heinrich","year":"1981","journal-title":"J. Exp. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"395","DOI":"10.2307\/1310562","article-title":"Temperature control in honey bee colonies","volume":"37","author":"Southwick","year":"1987","journal-title":"Bioscience"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1007\/s00114-002-0338-7","article-title":"Hot spots in the bee hive","volume":"89","author":"Bujok","year":"2002","journal-title":"Naturwissenschaften"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/0300-9629(82)90400-5","article-title":"Metabolic energy of intact honey bee colonies","volume":"71","author":"Southwick","year":"1982","journal-title":"Comp Biochem. Physiol. A"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.jtherbio.2005.12.005","article-title":"The development of the concepts of homeothermy and thermoregulation","volume":"31","author":"Ivanov","year":"2006","journal-title":"J. Therm. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1007\/s001140050709","article-title":"Fever in honeybee colonies","volume":"87","author":"Starks","year":"2000","journal-title":"Naturwissenschaften"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"789","DOI":"10.3390\/insects3030789","article-title":"Behavioral immunity in insects","volume":"3","year":"2012","journal-title":"Insects"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Goblirsch, M., Warner, J.F., Sommerfeldt, B.A., and Spivak, M. (2020). Social fever or general immune response? Revisiting an example of social immunity in honey bees. Insects, 11.","DOI":"10.3390\/insects11080528"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/j.jtherbio.2018.04.012","article-title":"Recognition of mite-infested brood by honeybee (Apis mellifera) workers may involve thermal sensing","volume":"74","author":"Bauer","year":"2018","journal-title":"J. Therm. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Sipos, T., Donk\u00f3, T., J\u00f3cs\u00e1k, I., and Keszthelyi, S. (2021). Study of Morphological Features in Pre-Imaginal Honey Bee Impaired by Varroa destructor by Means of Computer Tomography. Insects, 12.","DOI":"10.3390\/insects12080717"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"108109","DOI":"10.1016\/j.jip.2024.108109","article-title":"Analysis of X-ray irradiation effects on the mortality values and hemolymph immune cell composition of Apis mellifera and its parasite, Varroa destructor","volume":"204","author":"Sipos","year":"2024","journal-title":"J. Invertebr. Pathol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/S0968-4328(01)00010-5","article-title":"Biological infrared imaging and sensing","volume":"33","author":"Campbell","year":"2002","journal-title":"Micron"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"181281","DOI":"10.1098\/rsos.181281","article-title":"Reporting of thermography parameters in biology: A systematic review of thermal imaging literature","volume":"5","author":"Harrap","year":"2018","journal-title":"R. Soc. Open Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1007\/s12206-022-0144-4","article-title":"Skin temperature characteristics of the ligustrum moth (Brahmaea certhia) and the hawk moth (Theretra oldenlandiae) using IR camera","volume":"36","author":"Kim","year":"2022","journal-title":"J. Mech. Sci. Technol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.tca.2012.02.006","article-title":"Assessing honeybee and wasp thermoregulation and energetics\u2014New insights by combination of flow-through respirometry with infrared thermography","volume":"534","author":"Stabentheiner","year":"2012","journal-title":"Thermochim. Acta"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"104898","DOI":"10.1016\/j.compag.2019.104898","article-title":"A computer vision system to monitor the infestation level of Varroa destructor in a honeybee colony","volume":"164","author":"Bjerge","year":"2019","journal-title":"Comput. Electron. Agric."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1080\/00450618.2013.793740","article-title":"Infrared imaging as a non-invasive tool for documenting maggot mass temperatures","volume":"46","author":"Johnson","year":"2014","journal-title":"Aust. J. Forensic Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/j.jtherbio.2011.07.008","article-title":"Application of infrared thermography to the study of behavioural fever in the desert locust","volume":"36","author":"Hunt","year":"2011","journal-title":"J. Therm. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Klein, B.A., Stiegler, M., Klein, A., and Tautz, J. (2014). Mapping sleeping bees within their nest: Spatial and temporal analysis of worker honey bee sleep. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0102316"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1051\/apido:19800104","article-title":"Characterization of postembryonic developmental stages of the female castes of the honey bee, Apis mellifera L.","volume":"11","author":"Rembold","year":"1980","journal-title":"Apidologie"},{"key":"ref_33","first-page":"1","article-title":"Standard methods for varroa research","volume":"52","author":"Dietemann","year":"2013","journal-title":"J. Apic. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"109359","DOI":"10.1016\/j.ecolmodel.2020.109359","article-title":"Population dynamics of Varroa mite and honeybee: Effects of parasitism with age structure and seasonality","volume":"440","author":"Messan","year":"2021","journal-title":"Ecol. Model."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"107890","DOI":"10.1016\/j.jip.2023.107890","article-title":"Varroa destructor re-invasion dynamics during autumn and winter in Apis mellifera colonies from a temperate climate","volume":"197","author":"Giacobino","year":"2023","journal-title":"J. Invertebr. Pathol."},{"key":"ref_36","first-page":"125","article-title":"Nectar production for the Hungarian honey industry","volume":"1","author":"Farkas","year":"2007","journal-title":"Eur. J. Plant Sci. Biotechnol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Peck, D.T., and Seeley, T.D. (2019). Mite bombs or robber lures? The roles of drifting and robbing in Varroa destructor transmission from collapsing honey bee colonies to their neighbors. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0218392"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Bava, R., Castagna, F., Palma, E., Ceniti, C., Millea, M., Lupia, C., Britti, D., and Musella, V. (2023). Prevalence of Varroa destructor in honeybee (Apis mellifera) farms and varroosis control practices in Southern Italy. Microorganisms, 11.","DOI":"10.3390\/microorganisms11051228"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"S96","DOI":"10.1016\/j.jip.2009.07.016","article-title":"Biology and control of Varroa destructor","volume":"103","author":"Rosenkranz","year":"2010","journal-title":"J. Invertebr. Pathol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"601","DOI":"10.3390\/insects3030601","article-title":"How Varroa parasitism affects the immunological and nutritional status of the honey bee, Apis mellifera","volume":"3","author":"Aronstein","year":"2012","journal-title":"Insects"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e9583","DOI":"10.7717\/peerj.9583","article-title":"Slumber in a cell: Honeycomb used by honey bees for food, brood, heatin and sleeping","volume":"8","author":"Klein","year":"2020","journal-title":"PeerJ"},{"key":"ref_42","unstructured":"Fermi, E. (2012). Thermodynamics, Courier Corporation."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Lee, J.H., and Ramamurthi, K. (2022). Fundamentals of Thermodynamics, CRC Press.","DOI":"10.1201\/9781003224044"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1007\/s13592-020-00738-5","article-title":"Body mass of honey bee drones developing in constant and in changing temperatures","volume":"51","author":"Tofilski","year":"2020","journal-title":"Apidologie"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4217","DOI":"10.1242\/jeb.00680","article-title":"Hot bees in empty broodnest cells: Heating from within","volume":"206","author":"Kleinhenz","year":"2003","journal-title":"J. Exp. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1046\/j.1365-3032.2002.00284.x","article-title":"Potential mechanism for detection by Apis mellifera of the parasitic mite Varroa destructor inside sealed brood cells","volume":"27","author":"Martin","year":"2002","journal-title":"Physiol. Entomol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1007\/s10493-020-00519-w","article-title":"Varroa destructor mite electrophysiological responses to honey bee (Apis mellifera) colony volatiles","volume":"81","author":"Light","year":"2020","journal-title":"Exp. Appl. Acarol."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/15\/9\/693\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:55:37Z","timestamp":1760111737000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/15\/9\/693"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,13]]},"references-count":47,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,9]]}},"alternative-id":["insects15090693"],"URL":"https:\/\/doi.org\/10.3390\/insects15090693","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,13]]}}}